AUTHOR=Khadka Roshan , Clothier Lindsay , Wang Lin , Lim Chee Kent , Klotz Martin G. , Dunfield Peter F. 

TITLE=Evolutionary History of Copper Membrane Monooxygenases

JOURNAL=Frontiers in Microbiology

VOLUME=9

YEAR=2018

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2018.02493

DOI=10.3389/fmicb.2018.02493

ISSN=1664-302X

ABSTRACT=<p>Copper membrane monooxygenases (CuMMOs) oxidize ammonia, methane and some short-chain alkanes and alkenes. They are encoded by three genes, usually in an operon of <italic>xmoCAB</italic>. We aligned <italic>xmo</italic> operons from 66 microbial genomes, including members of the <italic>Alpha</italic>-, <italic>Beta</italic>-, and <italic>Gamma-proteobacteria, Verrucomicrobia, Actinobacteria, Thaumarchaeota</italic> and the candidate phylum NC10. Phylogenetic and compositional analyses were used to reconstruct the evolutionary history of the enzyme and detect potential lateral gene transfer (LGT) events. The phylogenetic analyses showed at least 10 clusters corresponding to a combination of substrate specificity and bacterial taxonomy, but with no overriding structure based on either function or taxonomy alone. Adaptation of the enzyme to preferentially oxidize either ammonia or methane has occurred more than once. Individual phylogenies of all three genes, <italic>xmoA, xmoB</italic> and <italic>xmoC</italic>, closely matched, indicating that this operon evolved or was consistently transferred as a unit, with the possible exception of the methane monooxygenase operons in <italic>Verrucomicrobia</italic>, where the <italic>pmoB</italic> gene has a distinct phylogeny from <italic>pmoA</italic> and <italic>pmoC</italic>. Compositional analyses indicated that some clusters of <italic>xmoCAB</italic> operons (for example, the <italic>pmoCAB</italic> in gammaproteobacterial methanotrophs and the <italic>amoCAB</italic> in betaproteobacterial nitrifiers) were compositionally very different from their genomes, possibly indicating recent lateral transfer of these operons. The combined phylogenetic and compositional analyses support the hypothesis that an ancestor of the nitrifying bacterium <italic>Nitrosococcus</italic> was the donor of methane monooxygenase (pMMO) to both the alphaproteobacterial and gammaproteobacterial methanotrophs, but that before this event the gammaproteobacterial methanotrophs originally possessed another CuMMO (Pxm), which has since been lost in many species.</p>